Floral trait variation across individual plants within a population enhances defense capability to nectar robbing

doi:10.1016/j.pld.2022.11.002

Plant Diversity ›› 2023, Vol. 45 ›› Issue (03): 315-325.DOI: 10.1016/j.pld.2022.11.002

Floral trait variation across individual plants within a population enhances defense capability to nectar robbing

Shuang Tie^a, Yong-Deng He^b,c,d, Amparo Lázaro^e, David W. Inouye^f,g, You-Hao Guo^a, Chun-Feng Yang^b,c

a. College of Life Sciences, Wuhan University, Wuhan 430072, China;
b. CAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China;
c. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan 430074, China;
d. University of Chinese Academy of Sciences, Beijing 100049, China;
e. Global Change Research Group, Mediterranean Institute for Advanced Studies (IMEDEA; UIB-CSIC), Esporles, Balearic Islands, Spain;
f. The Rocky Mountain Biological Laboratory, Post Office Box 519, Crested Butte, CO 81224, USA;
g. Department of Biology, University of Maryland, College Park, MD 20742, USA

收稿日期:2022-06-10 修回日期:2022-11-01 发布日期:2023-07-06
通讯作者: You-Hao Guo,E-mail:yhguo@whu.edu.cn;Chun-Feng Yang,E-mail:cfyang@wbgcas.cn
基金资助:
We thank Ming-Fang Du for assistance in the field, Jia-Xing Huang for identifying the bumble bees, and Michele Dudash for improvement on an earlier manuscript. The research was supported by the National Natural Science Foundation of China (No. 31970253 and 32270243) and the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB31010000). AL was also supported by a Ramón y Cajal contract (RYC-2015-19034) from the Spanish Ministry of Science, Innovation and Universities, the Spanish State Research Agency, European Social Funds (ESF invests in your future) and the University of the Balearic Islands, and by the project PRPPID2020-117863RB-I00, financed by the Spanish Ministry of Science and Innovation and the Spanish Research Agency (MCIN/AEI/10.13039/501100011033).

Floral trait variation across individual plants within a population enhances defense capability to nectar robbing

Shuang Tie^a, Yong-Deng He^b,c,d, Amparo Lázaro^e, David W. Inouye^f,g, You-Hao Guo^a, Chun-Feng Yang^b,c

a. College of Life Sciences, Wuhan University, Wuhan 430072, China;
b. CAS Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden, Chinese Academy of Sciences, Wuhan 430074, China;
c. Center of Conservation Biology, Core Botanical Gardens, Chinese Academy of Sciences, Wuhan 430074, China;
d. University of Chinese Academy of Sciences, Beijing 100049, China;
e. Global Change Research Group, Mediterranean Institute for Advanced Studies (IMEDEA; UIB-CSIC), Esporles, Balearic Islands, Spain;
f. The Rocky Mountain Biological Laboratory, Post Office Box 519, Crested Butte, CO 81224, USA;
g. Department of Biology, University of Maryland, College Park, MD 20742, USA

Received:2022-06-10 Revised:2022-11-01 Published:2023-07-06
Contact: You-Hao Guo,E-mail:yhguo@whu.edu.cn;Chun-Feng Yang,E-mail:cfyang@wbgcas.cn
Supported by:
We thank Ming-Fang Du for assistance in the field, Jia-Xing Huang for identifying the bumble bees, and Michele Dudash for improvement on an earlier manuscript. The research was supported by the National Natural Science Foundation of China (No. 31970253 and 32270243) and the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB31010000). AL was also supported by a Ramón y Cajal contract (RYC-2015-19034) from the Spanish Ministry of Science, Innovation and Universities, the Spanish State Research Agency, European Social Funds (ESF invests in your future) and the University of the Balearic Islands, and by the project PRPPID2020-117863RB-I00, financed by the Spanish Ministry of Science and Innovation and the Spanish Research Agency (MCIN/AEI/10.13039/501100011033).

摘要/Abstract

摘要： Floral trait variation may help pollinators and nectar robbers identify their target plants and, thus, lead to differential selection pressure for defense capability against floral antagonists. However, the effect of floral trait variation among individuals within a population on multi-dimensional plant-animal interactions has been little explored. We investigated floral trait variation, pollination, and nectar robbing among individual plants in a population of the bumble bee-pollinated plant, Caryopteris divaricata, from which flowers are also robbed by bumble bees with varying intensity across individuals. We measured the variation in corolla tube length, nectar volume and sugar concentration among individual plants, and evaluated whether the variation were recognized by pollinators and robbers. We investigated the influence of nectar robbing on legitimate visitation and seed production per fruit. We found that the primary nectar robber (Bombus nobilis) preferred to forage on plants with long-tubed flowers, which produced less nectar and had lower sugar concentration compared to those with shorter corolla tubes. Individuals with shorter corolla tubes had comparatively lower nectar robbing intensity but higher visitation by legitimate visitors (mainly B. picipes) and higher seed production. Nectar robbing significantly reduced seed production because it decreased pollinator visits. However, neither pollination nor seed production differed between plants with long and short corolla tubes when nectar robbers were excluded. This finding suggests that floral trait variation might not be driven by pollinators. Such variation among individual plants thus allows legitimate visitors and nectar robbers to segregate niches and enhances population defense against nectar robbing in unpredictable conditions.

关键词: Bumble bees, Caryopteris divaricata, Corolla tube, Intraspecific variation, Plant reproductive success, Pollination

Abstract: Floral trait variation may help pollinators and nectar robbers identify their target plants and, thus, lead to differential selection pressure for defense capability against floral antagonists. However, the effect of floral trait variation among individuals within a population on multi-dimensional plant-animal interactions has been little explored. We investigated floral trait variation, pollination, and nectar robbing among individual plants in a population of the bumble bee-pollinated plant, Caryopteris divaricata, from which flowers are also robbed by bumble bees with varying intensity across individuals. We measured the variation in corolla tube length, nectar volume and sugar concentration among individual plants, and evaluated whether the variation were recognized by pollinators and robbers. We investigated the influence of nectar robbing on legitimate visitation and seed production per fruit. We found that the primary nectar robber (Bombus nobilis) preferred to forage on plants with long-tubed flowers, which produced less nectar and had lower sugar concentration compared to those with shorter corolla tubes. Individuals with shorter corolla tubes had comparatively lower nectar robbing intensity but higher visitation by legitimate visitors (mainly B. picipes) and higher seed production. Nectar robbing significantly reduced seed production because it decreased pollinator visits. However, neither pollination nor seed production differed between plants with long and short corolla tubes when nectar robbers were excluded. This finding suggests that floral trait variation might not be driven by pollinators. Such variation among individual plants thus allows legitimate visitors and nectar robbers to segregate niches and enhances population defense against nectar robbing in unpredictable conditions.

Key words: Bumble bees, Caryopteris divaricata, Corolla tube, Intraspecific variation, Plant reproductive success, Pollination

Shuang Tie, Yong-Deng He, Amparo Lázaro, David W. Inouye, You-Hao Guo, Chun-Feng Yang. Floral trait variation across individual plants within a population enhances defense capability to nectar robbing[J]. Plant Diversity, 2023, 45(03): 315-325.

参考文献

[1] Armbruster, W.S., 2017. The specialization continuum in pollination systems:diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31, 88-100.
[2] Bangert, R.K., Turek, R.J., Martinsen, G.D., et al., 2005. Benefits of conservation of plant genetic diversity to arthropod diversity. Conserv. Biol. 19, 379-390.
[3] Barker, J.L., Dornhaus, A., Bronstein, J.L., Muth, F., 2018. Learning about larceny:experience can bias bumble bees to rob nectar. Behav. Ecol. Sociobiol. 72, 1-11.
[4] Barton, K., 2019. MuMIn:Multi-Model Inference. R package version 1.43.15. https://CRAN.R-project.org/package=MuMIn
[5] Bates, D., Maechler, M., Bolker, B., et al., 2015. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1-48.
[6] Benadi, G., Pauw, A., 2018. Frequency dependence of pollinator visitation rates suggests that pollination niches can allow plant species coexistence. J. Ecol. 106, 1892-1901.
[7] Bronstein, J.L., Barker, J.L., Lichtenberg, E.M., et al., 2017. The behavioral ecology of nectar robbing:why be tactic constant? Curr. Opin. Insect. Sci. 21, 14-18.
[8] Brooks, M.E., Kristensen, K., Van, B.K.J., et al., 2017. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R Journal 9, 378-400.
[9] Cantino, P.D., Wagstaff, S.J., Olmstead, R.G., 1999. Caryopteris (Lamiaceae) and the conflict between phylogenetic and pragmatic considerations in botanical nomenclature. Syst. Bot. 23, 369-386.
[10] Chalcoff, V.R., Aizen, M.A., Galetto, L., 2006. Nectar concentration and composition of 26 species from the temperate forest of South America. Ann. Bot. 97, 413-421.
[11] Consul, P.C., 1989. Generalized Poisson distributions:properties and applications. New York, NY:Marcel Dekker.
[12] Consul, P.C., Famoye, F., 1992. Generalized Poisson regression model. Commun. Stat. -Theory Methods 21, 89-109.
[13] Delesalle, V.A., Mazer, S.J., 1995. The structure of phenotypic variation in gender and floral traits within and among populations of Spergularia marina (Caryophyllaceae). Am. J. Bot. 82, 798-810.
[14] Fox, J., Weisberg, S., 2019. An {R} Companion to Applied Regression, Third Edition. Thousand Oaks CA:Sage. URL:https://socialsciences.mcmaster.ca/jfox/Books/Companion/
[15] Galen, C., Cuba, J., 2001. Down the tube:pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55, 1963-1971.
[16] Galen, C., 1999. Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. Bioscience 49, 631-640.
[17] Goulson, D., 1999. Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect. Plant. Ecol. Evol. Syst. 2, 185-209.
[18] Grant, V., 1949. Pollination systems as isolating mechanisms in angiosperms. Evolution 3, 82-97.
[19] Harder, L.D., 1986. Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69, 309-315.
[20] Hartig, F., 2021. DHARMa:residual diagnostics for hierarchical (Multi-Level/mixed) regression models. R package version 0.4.1.https://CRAN.R-project.org/package=DHARMa
[21] Huang, J.G., Ma, Q., Rossi, S., et al., 2020. Photoperiod and temperature as dominant environmental drivers triggering secondary growth resumption in Northern Hemisphere conifers. Proc. Natl. Acad. Sci. U. S. A. 117, 20645-20652.
[22] Hughes, A.R., Inouye, B.D., Johnson, M.T., et al., 2008. Ecological consequences of genetic diversity. Ecol. Lett. 11, 609-623.
[23] Inouye, D.W., 1980. The terminology of floral larceny. Ecology 61, 1251-1253.
[24] Irwin, R.E., Bronstein, J.L., Manson, J.S., et al., 2010. Nectar robbing:ecological and evolutionary perspectives. Annu. Rev. Ecol. Evol. Syst. 41, 271-292.
[25] Irwin, R.E., Maloof, J.E., 2002. Variation in nectar robbing over time, space, and species. Oecologia 133, 525-533.
[26] Ishii, H.S., Kadoya, E.Z., 2016. Legitimate visitors and nectar robbers on Trifolium pratense showed contrasting flower fidelity versus co-flowering plant species:could motor learning be a major determinant of flower constancy by bumble bees? Behav. Ecol. Sociobiol. 70, 377-386.
[27] Jacquemyn, H., Brys, R., 2020. Lack of strong selection pressures maintains wide variation in floral traits in a food-deceptive orchid. Ann. Bot. 126, 445-453.
[28] Johnson, D., Martin, F., Cairney, J.W., et al., 2012. The importance of individuals:intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New. Phytol. 194, 614-628.
[29] Jump, A.S., Marchant, R., Penuelas, J., 2009. Environmental change and the option value of genetic diversity. Trends Plant Sci. 14, 51-58.
[30] Kohl, P.L., Steffan-Dewenter, I., 2022. Nectar robbing rather than pollinator availability constrains reproduction of a bee-flowered plant at high elevations. Ecosphere 13, e4077.
[31] Lara, C., Ornelas, J.F., 2001. Preferential nectar robbing of flowers with long corollas:experimental studies of two humming-bird species visiting three plant species. Oecologia 128, 263-273.
[32] Lazaro, A., Vignolo, C., Santamaria, L., 2015. Long corollas as nectar barriers in Lonicera implexa:interactions between corolla tube length and nectar volume. Evol. Ecol. 29, 419-435.
[33] Lichtenberg, E.M., Irwin, R.E., Bronstein, J.L., 2020a. Bumble bees are constant to nectar-robbing behaviour despite low switching costs. Anim. Behav. 170, 177-188.
[34] Lichtenberg, E.M., Richman, S.K., Irwin, R.E., et al., 2020b. Competition for nectar resources does not affect bee foraging tactic constancy. Ecol. Entomol. 45, 904-909.
[35] Maruyama, P.K., Vizentin-Bugoni, J., Dalsgaard, B., et al., 2015. Nectar robbery by a hermit hummingbird:association to floral phenotype and its influence on flowers and network structure. Oecologia 178, 783-793.
[36] Mendez-Vigo, B., Gomaa, N.H., Alonso-Blanco, C., et al., 2013. Among- and within-population variation in flowering time of Iberian Arabidopsis thaliana estimated in field and glasshouse conditions. New. Phytol. 197, 1332-1343.
[37] Nardone, E., Dey, T., Kevan, P.G., 2013. The effect of sugar solution type, sugar concentration and viscosity on the imbibition and energy intake rate of bumblebees. J. Insect Physiol. 59, 919-933.
[38] Pattrick, J.G., Symington, H.A., Federle, W., et al., 2020. The mechanics of nectar offloading in the bumblebee Bombus terrestris and implications for optimal concentrations during nectar foraging. J. R. Soc. Interface 17, 20190632.
[39] Pei, C., Chen, S.L. (Eds.), 1982. FLORA Reipublicae Popularis Sinicae:Volume 65:Verbenaceae. Beijing:Science Press.
[40] R Core Team, 2019. R:A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
[41] Raffard, A., Santoul, F., Cucherousset, J., et al., 2019. The community and ecosystem consequences of intraspecific diversity:a meta-analysis. Biol. Rev. 94, 648-661.
[42] Richman, S.K., Irwin, R.E., Nelson, C.J., et al., 2017. Facilitated exploitation of pollination mutualisms:fitness consequences for plants. J. Ecol. 105, 188-196.
[43] Rojas-Nossa, S.V., Sanchez, J.M., Navarro, L., 2016. Nectar robbing:a common phenomenon mainly determined by accessibility constraints, nectar volume and density of energy rewards. Oikos 125, 1044-1055.
[44] Rojas-Nossa, S.V., Sanchez, J.M., Navarro, L., 2021. Nectar robbing and plant reproduction:an interplay of positive and negative effects. Oikos 130, 601-608.
[45] Stoffel, M.A., Nakagaw, S., Schielzeth, H., 2020. partR2:Partitioning R2 in generalized linear mixed models. bioRxiv doi:10.1101/2020.07.26.221168
[46] Sutherland, W.J., Freckleton, R.P., Godfray, H.C.J., et al., 2012. Identification of 100 fundamental ecological questions. J. Ecol. 101, 58-67.
[47] Whittall, J.B., Hodges, S.A., 2007. Pollinator shifts drive increasingly long nectar spursin columbine flowers. Nature 447, 706-709.
[48] Yang, C.F., Wang, Q.F., 2015. Nectarless flowers with deep corolla tubes in Pedicularis:does long pistil length provide an arena for male competition? Bot. J. Linn. Soc. 179, 526-532.
[49] Ye, Z.M., Jin, X.F., Inouye, D.W., et al., 2018. Variation in composition of two bumble bee species across communities affects nectar robbing but maintains pollinator visitation rate to an alpine plant, Salvia przewalskii. Ecol. Entomol. 43, 363-370.
[50] Ye, Z.M., Jin, X.F., Wang, Q.F., et al., 2017. Nectar replenishment maintains the neutraleffects of nectar robbing on female reproductive success of Salvia przewalskii (Lamiaceae), a plant pollinated and robbed by bumble bees. Ann. Bot. 119:1053-1059.
[51] Zeileis, A., Kleiber, C., Jackman, S., 2008. Regression models for count data in R. J. Stat. Software 27, 1-25. http://www.jstatsoft.org/v27/i08/.
[52] Zeileis, A., Hothorn, T., 2002. Diagnostic checking in regression relationships. R. News 2, 7-10. URLhttps://CRAN.R-project.org/doc/Rnews/.
[53] Zuur, A.F., Ieno, E.N., 2016. Beginner's Guide to Zero-Inflated Models with R Newburgh:Highland Statistics Ltd.

Floral trait variation across individual plants within a population enhances defense capability to nectar robbing

Floral trait variation across individual plants within a population enhances defense capability to nectar robbing

PDF (PC)

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 12

编辑推荐

Metrics

本文评价

[1]	Pisal Chheang, David H. Hembry, Gang Yao, Shi-Xiao Luo. Diversity and species-specificity of brood pollination of leafflower trees (Phyllanthaceae: Glochidion) by leafflower moths (Lepidoptera: Epicephala) in tropical Southeast Asia (Cambodia)[J]. Plant Diversity, 2022, 44(02): 191-200.
[2]	Harue Abe, Hiroki Miura, Yoshitaka Motonaga. Quantitative classification of Camellia japonica and Camellia rusticana (Theaceae) based on leaf and flower morphology[J]. Plant Diversity, 2021, 43(03): 216-224.
[3]	Wumei Xu, Kyle W. Tomlinson, Jie Li. Strong intraspecific trait variation in a tropical dominant tree species along an elevational gradient[J]. Plant Diversity, 2020, 42(01): 1-6.
[4]	Zhi-Li Zhou, Yuan-Wen Duan, Yan Luo, Yong-Ping Yang, Zhi-Qiang Zhang. Cell number explains the intraspecific spur-length variation in an Aquilegia species[J]. Plant Diversity, 2019, 41(05): 307-314.
[5]	ysajan Abdusalam, Qing Jun Li. Elevation-related variation in the population characteristics of distylous Primula nivalis affects female fitness and inbreeding depression[J]. Plant Diversity, 2019, 41(04): 250-257.
[6]	Zongxin Ren, Yanhui Zhao, Huan Liang, Zhibin Tao, Hui Tang, Haiping Zhang, Hong Wang. Pollination ecology in China from 1977 to 2017[J]. Plant Diversity, 2018, 40(04): 172-180.
[7]	Juan Yan, Menglin Wang, Ling Zhang. Light induces petal color change in Quisqualis indica (Combretaceae)[J]. Plant Diversity, 2018, 40(01): 28-34.
[8]	Xinmin Zhang, Darong Yang. Occurrence of internally ovipositing non-agaonid wasps and pollination mode of the associated agaonid wasps[J]. Plant Diversity, 2017, 39(03): 130-134.
[9]	Bin Wang, Gao Chen, Congren Li, Weibang Sun. Floral characteristics and pollination ecology of Manglietia ventii (Magnoliaceae), a plant species with extremely small populations (PSESP) endemic to South Yunnan of China[J]. Plant Diversity, 2017, 39(01): 52-59.
[10]	Yahuang Luo, Jie Liu, Shaolin Tan, Marc W. Cadotte, Kun Xu, Lianming Gao, Dezhu Li. Trait variation and functional diversity maintenance of understory herbaceous species coexisting along an elevational gradient in Yulong Mountain, Southwest China[J]. Plant Diversity, 2016, 38(06): 303-311.
[11]	Ye Chen, Gao Chen, Jing Yang, Weibang Sun. Reproductive biology of Magnolia sinica (Magnoliaecea), a threatened species with extremely small populations in Yunnan, China[J]. Plant Diversity, 2016, 38(05): 253-258.
[12]	Gao Chen, Changqiu Liu, Weibang Sun. Pollination and seed dispersal of Aquilaria sinensis (Lour.) Gilg (Thymelaeaceae): An economic plant species with extremely small populations in China[J]. Plant Diversity, 2016, 38(05): 227-232.